REVIEW

Introduction of Mandshurian ash (Fraxinus mandshurica Rupr.)to Estonia: Is it related to the current epidemic on European ash(F. excelsior L.)?

Rein Drenkhan • Heldur Sander • Mart Hanso

Received: 18 December 2013 / Revised: 26 March 2014 / Accepted: 28 March 2014

� Springer-Verlag Berlin Heidelberg 2014

Abstract Recent investigations in Japan have suggested

that the causal organism of the ongoing epidemic affecting

European ash (Fraxinus excelsior) in Europe, Hymenosc-

yphus pseudoalbidus, may originate in East Asia. The

fungus may have been unintentionally carried to Europe

during the introduction of Mandshurian ash (F. mandshu-

rica), the host tree of the fungus in East Asia. Still uni-

centric emergence hypothesis is in force: An area in the

eastern Poland or Baltic has been shown to be the pre-

sumed epicentre of the epidemic. Really, during the Soviet

occupation, several consignments of F. mandshurica seeds

and plants, originating directly from the natural range of F.

mandshurica in East Asia (Russian Far East), reached

Baltic areas. In this paper, an overview about the Mand-

shurian ash is presented, the history of introduction of F.

mandshurica to Estonia is reviewed and colonization of F.

excelsior in this country by H. pseudoalbidus is briefly

discussed. At present, we could not find any evidence,

spatial or temporal, for a direct connection of the disease

emergence on native F. excelsior with the introduction of

F. mandshurica. The pathogen first colonized northwest

Estonia and moved southeast and not from south to north as

would be expected according to the hitherto existing uni-

centric hypothesis. However, more information is needed

from different regions before to pose a multicentric emer-

gence hypothesis and to deepen more into the investiga-

tions of the environmental factors that affected the host and

supported to the epidemic in different areas.

Keywords Ash dieback � Hymenoscyphus

pseudoalbidus � Chalara fraxinea � Russian Far East �Introduction history � Emergence of epidemic

Introduction

Undoubtedly, the European ash (Fraxinus excelsior L.) die-

back is currently the most acute forest pathology problem in

Europe, representing a major threat to the European forestry

and biodiversity (Pautasso et al. 2013). Recently, it was sug-

gested in Europe (Queloz et al. 2011) and demonstrated by

molecular methods in Japan (Zhao et al. 2012) that the agent

of the epidemic Hymenoscyphus pseudoalbidus Queloz,

Grunig, Berndt, Kowalski, Lieber et Holdenrieder may orig-

inate in East Asia. Locating the geographical epicentre of the

disease in Europe and reconstruction of the invasion routes

and pathways of the movement of its pathogen from East Asia

to Europe and of subsequent dissemination here are pressing

research needs (Pautasso et al. 2013; Gross et al. 2014).

As one possible invasion route, the pathogen may have

been unintentionally carried to Europe during the intro-

duction of Mandshurian ash (F. mandshurica), the host tree

of the fungus in East Asia (Zhao et al. 2012).

Until today, an unicentric emergence hypothesis is

existing: As yet unspecified area around the Baltic Sea

(Dobrowolska et al. 2011) or in the south Baltic and eastern

Poland, or only eastern Poland (Juodvalkis and Vasiliaus-

kas 2002; Przybył 2002; Vasiliauskas et al. 2002; Sku-

odiene et al. 2003; Kowalski and Łukomska 2005;

Thomsen et al. 2009; Timmermann et al. 2011; Gross et al.

2014) has been shown to be the presumed core colonization

centre for the pathogen, which thereafter spread to the

west, north and south (Kirisits et al. 2009; Thomsen et al.

2009; Timmermann et al. 2011; Gross et al. 2014).

Communicated by J. Holopainen.

R. Drenkhan (&) � H. Sander � M. Hanso

Institute of Forestry and Rural Engineering, Estonian University

of Life Sciences, Fr.R. Kreutzwaldi 5, 51014 Tartu, Estonia

e-mail: rein.drenkhan@emu.ee

123

Eur J Forest Res

DOI 10.1007/s10342-014-0811-9

During the decades of Soviet occupation in Baltic

countries, especially from the 1960s to the 1980s, several

consignments of F. mandshurica, originating directly from

the natural range of F. mandshurica in East Asia (in the

Russian Far East), were brought and planted in Baltic

areas. These consignments consisted mainly of seeds, but

sometimes also of young plants. Currently, the natural

infection of seeds by the fungus was demonstrated by

Cleary et al. (2013), increasing the probability of accidental

long-distance transmissions of the fungus.

Presumably, the Baltic countries were the main domain

in Europe where Mandshurian ash was directly planted

after movement from its natural range. However, there is

no known literature data regarding possible plantings in

Kaliningrad and Belarus, which also are inside or near to

the presumed up today single epicentre (Fig. 1, B), and

which also were at that time part of the Soviet Union and

thus subject to unimpeded movement of living plant

materials.

It should be mentioned that, up to this point, no infor-

mation is available about the occurrence or abundance of

the fungus on F. mandshurica in the Russian Far East, still

the fungus has been documented in Japan (Zhao et al.

2012) and, currently, in north-eastern China (Zheng and

Zhuang 2013). In Japan and in China, H. pseudoalbidus has

not caused losses to its host, F. mandshurica (Zhao et al.

2012, Zheng and Zhuang 2013). This demonstrates that it is

often difficult to predict if a fungus can become invasive

and cause epidemics in new areas.

Analysis of historical data is an essential tool for iden-

tifying invasion pathways (Britton and Liebhold 2013). A

better use of arboreta in identification of the causes of death

of exotic woody plants, keeping samples in herbarium and

collections for further investigations are strongly recom-

mended today in pest risk assessment (Tomoshevich et al.

2013). Obviously, the natural distribution, ecology, but also

history and silvicultural experience of the introduction of

Mandshurian ash (F. mandshurica) in different areas are

essential issues of the problem. The aim of this review was

to collect the disparate information: (1) for characterization

of Mandshurian ash in East Asia, (2) about the introduction

history of this exotic ash species to Estonia, (3) to explore

the background of its introductions to the other areas of the

former Russian empire and former Soviet Union and (4)

the spatial and temporal juxtaposition of the occurrence of

Mandshurian ash (F. mandshurica) with the disease

Fig. 1 Introduction history of Mandshurian ash (F. mandshurica) to

Estonia (and to some other destinations). Hatched areas: A—

approximate natural range of Mandshurian ash, B—presumed

epicentre area of the European ash dieback in Europe. Year numbers

on the arrow—direct introduction years of F. mandshurica to Estonia.

Approximate location of the other known introduction points: 1—St.

Petersburg, 2—Komi (near Syktyvkar), 3—Moscow, 4—Krasnoy-

arsk, 5—Kasakhstan, 6—Usbekistan, 7—Turkmenistan

Eur J Forest Res

123

emergence and survey data in indigenous European ash (F.

excelsior) in Estonia and in close environs.

The only area of origin of F. mandshurica during the

entire history of introduction to Estonia has been the

Russian Far East. Since most papers about this area have

been written in Russian and information about these papers

was poorly accessible to foreign readers (Koponen and

Koponen 1995, Krestov 2003), a review of the natural

range and behaviour of Mandshurian ash ‘‘at home’’ is

presented in this paper, largely based on the Russian-lan-

guage literature.

Mandshurian ash (Fraxinus mandshurica)

Fraxinus mandshurica Rupr. (F. mandshurica var. mand-

shurica) Rupr. 1857 type specimen (isotype), collected by

Richard Maack in 1855 from the ‘‘Amurland’’ (Russian Far

East), is deposited in the herbarium of Harvard University

(Harvard University Herbaria Barcode GH00073884).

Richard Maack (1825–1886), an explorer and naturalist in

Russia and son of a Baltic German family, was born in Ku-

ressaare, Estonia (Tammiksaar 2005).

The first description of F. mandshurica was given in

1857 (Ruprecht 1857). Later, a Japanese variety F. mand-

shurica var. japonica Maxim. was separated from the

isotype (Maximovicz 1875).

Extent of the natural range of Mandshurian ash

North-eastern China comprises most of the central, and all

of the southern and nearly all of the western part of the

natural range of the Mandshurian ash (Hu et al. 2008). The

Russian Far East occupies the north-eastern and a small

part of the central area of the disjunctive natural range of

the species. The overall range is divided by the Strait of

Tatar and the northern part of the Japanese Sea, and

extends, in addition to north-eastern China and Russian Far

East, to North Korea and northern half of Japan (Fig. 1, A).

F. mandshurica is distributed in the Russian Far East

widely but discontinuously in Primorye and Priamurye, on

Sakhalin (in the southern half of the island) and in the

southernmost Kuril islands. Throughout all of the

Mandshuria (i.e. Zee-Bureinsk, Udsk, Ussur, Sakhalin) and

in riparian forests on the banks of the Amur River and its

headwaters, F. mandshurica is more abundant mainly in

river valleys (Vasilyev 1952). The borders of the range of

F. mandshurica in the Russian Far East are actually much

more meandering, and therefore, the total area of the range

is much smaller than that shown on Fig. 1, A, the last

crossing also sea aquatories.

The north-eastern border of the natural range of this

species at the geographical longitudes of Sakhalin and the

Kuril Islands coincides with the north-eastern border of the

southern boreal and hemiboreal vegetation zones of

Hamet-Ahti et al. (1974, see Fig. 2, SB/HB).

In the east, the region is bordered by the Pacific Ocean.

Along the coast, the natural range of F. mandshurica

reaches the town of Russkiy Gavan and down the Amur

River the town of Komsomolsk. In the north, its natural

range extends from the harbour of Russkiy Gavan (ca

49�N) and reaches the mountain chains of Large- and

Small-Hingan (in some parts extending up to 52�N). The

southern border is between 41� and 42�N on the coast, in

some places down to 39�N. As single trees or clusters of

small-size trees it can be found until the town Nikolayevsk.

Fig. 2 Horizontal bioclimatic vegetation zones in the coastal areas of

East Asia (Hamet-Ahti et al. 1974, supplemented): SB—southern

boreal zone, HB—hemiboreal zone, T—southern zone. Thick dotted

arcs—approximate north- and south-eastern border lines of the

natural range of F. mandshurica (orig.)

Eur J Forest Res

123

In the valley of the river Yasenevaya (in Russian: ash

river), close to the large estuary of the Amur River, grows a

relictic grove of F. mandshurica. The western and northern

borders of the natural range of this species extend from

Kumar on the Amur River and the source of the estuary of

the Tyrma River. Along the Selemdzcha River, the border

of the range reaches the estuary of the Nora River, along

Amguni—until at its mid-point, along Hora—until Sooli,

along Tumnin—through Tschitschimara (Usenko 1984).

Climate of the range and environmental requirements

of Mandshurian ash

The Russian Far East belongs to the monsoon region

(Ogureeva et al. 2012). The climate of that range is char-

acterized by the clash of air masses blowing from the huge

continental regions of Eurasia and similarly large air

masses from above the Pacific Ocean. Winters here are

influenced by the cold dry air masses from the interior of

East Asia, formed by the powerful Asian anticyclone. In

contrast, in the early summer, the southeast monsoon winds

bring cool and damp maritime air, but later in the summer

very damp, but warm air (Krestov 2003).

Mandshurian ash requires warm temperatures: even in

its home range, it can be damaged by late spring frosts

(Viryasov 1933). For the net photosynthetic rate, its opti-

mum air temperature was 28 �C, soil water potential

10 kPa, soil water content 23.4 % (Wenzhang et al. 1995).

Soil moisture content and late frosts are the main factors

limiting the growth of F. mandshurica in north-eastern

China (Su and Lin 2003). In a region of wetland forests in

Hokkaido, northern Japan, F. mandshurica had disappeared

from areas with negative soil redox potential (Yamamoto

et al. 1995).

Dendrofloristic characterization of the range

The Russian Far East is characterized by great floristic

dissimilarities (Hamet-Ahti et al. 1974). The range of F.

mandshurica here lies in 22 different dendrofloristic areas,

belonging to four dendrofloristic provinces of two larger

dendrofloristic regions: the Boreal and East Asian

(according to Nedolushko 1995, Fig. 3). In an earlier,

rougher classification (Viryasov 1933), the range was

divided into three floristic regions: Daurian, Mandshurian

and Ochota-Kamtchatsk.

Mandshurian ash is known as the most important

broadleaved timber tree and a key species under the climax

forest community in north-eastern China (Hu et al. 2008).

As single trees, F. mandshurica prefers mixed pine and

spruce forests (Vasilyev 1952).

Pinus koraiensis-broadleaved forests with admixture of

F. mandshurica in the Mandshurian dendrofloristic region

are rich in plant species (ca 2000, see Takhtajan 1986;

Nedolushko 1995, ref. after Petropavlovskiy et al. 2011),

and Mandshurian deciduous forests are gradually changing

into the Japanese–Chinese type forests. Its forest associa-

tions are closed, the shade-tolerant broadleaved tree species

often having 5–7 storeys. On the eastern slopes of the

Fig. 3 Dendrofloristic division of the part of Russian Far East

(according to Nedolushko 1995; cf. Petropavlovskiy et al. 2011,

supplemented), encompassing the northern and some central areas of

the natural range of Mandshurian ash (F. mandshurica): Boreal

dendrofloristic region, Ochotsko-Kamtschatskiy dendrofloristic prov-

ince (dendrofloristic areas: 14—Higher Bureinskiy, 15—Inferior

Amur, 16—Nordic Sichote-Alinskiy, 17—Nordic Sakhalin, 18—

Eastern Sakhalin, 20—Urupskiy); East Asian dendrofloristic region,

Mandshurian dendrofloristic province (dendrofloristic areas: 25—

Middle Zeiskiy, 26—Inferior Zeiskiy, 27—Inferior Bureinskiy, 28—

Birobidzhanskiy, 29—Amuro-Ussuriyskiy, 30—Middle Sichote-A-

linskiy, 32—Prihankaiskiy, 33—South-Primorskiy, 34—East-Prio-

morskiy), Sachalin-Hokkaido dendrofloristic province (dendrofloristic

areas: 35—Central Sakhalin, 36—South Sakhalin, 37—Krilyonskiy,

38—Iturupskiy, 39—Kunashir-Shikotanskiy). Thick dotted arc—

approximate north-eastern border line of the natural range of F.

mandshurica

Eur J Forest Res

123

Sikhote-Alini Mountains, Pinus koraiensis-broadleaf for-

ests grow up to the height of 150–700 m above sea level,

immediately neighbouring the belt of kseromesophilic

Mongolian oak (Quercus mongolica) forests (Ogureeva

et al. 2012).

The Mandshurian mixed forests most suitable for F.

mandshurica belong to the temperate mixed type. The veg-

etation type in this region with F. mandshurica as co-dom-

inant is broadleaved valley forest (Krestov 2003). Another

type of forests with F. mandshurica is northern Japanese

mixed forest in suboceanic southern Sakhalin and in the

southernmost Kuril Islands. In the mixed Abies sachalin-

ensis–Quercus crispula forest, an admixture of F. mand-

shurica can be also found. F. mandshurica reaches the upper

canopy layer there, among a dozen of other tree species.

The largest timber resources of F. mandshurica in the

Russian Far East are located in the basins of Anyuya, Kura,

Urmi and other headwaters of the Amur River (Usenko

1984). In mixed stands, F. mandshurica may comprise up

to 40–50 % of the total timber mass. Generally in its nat-

ural range, no pure stands of F. mandshurica can be found.

F. mandshurica trees reach a height of 25–30 m and a

diameter of 1 m, but on Sakhalin the species reaches a

height of 15 m. On dry and excessively moist soils, F.

mandshurica grows poorly (Usenko 1984).

Also in its southern and central range, i.e. in north-

eastern China (Hu et al. 2008), F. mandshurica grows

mainly in mixed forest communities. A substantial part of

the Pinus koraiensis-broadleaved forests is growing in the

Heilongjiang, Jilin and Ljaoning provinces of northeast

China. Until the middle of the last century, these forests

were reduced due to agricultural conversion (Ogureeva

et al. 2012). In secondary forests of mountain areas in

north-eastern China, this species can be found mixed with

many different tree species in different forest site types.

Some few pure F. mandshurica forests can be found only

along brooks (Wang 1995).

Current state of Mandshurian ash in its natural range

Old-growth forests in the Russian Far East have been

drastically reduced in the twentieth century as a result of

forest exploitation and fires (Krestov 2003). In China, F.

mandshurica is classified as endangered and is a national

priority protected tree species (Wang 1995). During the

investigation of spatiotemporal changes in the tree species

population sizes in natural forests, carried out from 1986 to

1994 on the north-eastern Chinese transect, it was estab-

lished that patch sizes of F. mandshurica had decreased

(Xiongwen et al. 2002). However, later investigations of

the responses of endangered tree species to the different

anthropogenic disturbances in mountain regions of north-

eastern China concluded that the distribution of Mand-

shurian ash remained unaffected (Zhu et al. 2007).

In the Republic of Korea, the natural Pinus koraiensis-

broadleaved forests have only remained in inaccessible

mountain regions, but by 2008 the area of the secondary

forests had reached already 320,000 ha (Ogureeva et al.

2012).

Genetic diversity within the populations of F. mand-

shurica in northeast China was found to be relatively high,

but slightly lower than other researchers had found for F.

mandshurica var. japonica in northern Japan and for F.

excelsior in Europe (Hu et al. 2008). The provenances of

Mandshurian ash from the southwest part of the north-

easternmost province of China, Heilongjiang, grow most

rapidly (Liu et al. 1997).

Generally, F. mandshurica is classified as a fast growing

and exceptionally wind-resistant species (Zhu et al. 2006),

but about 10 % of the mature trees of F. mandshurica in

the north of its natural range have trunk rot, caused mainly

by Inonotus hispidus and Pholiota mutabilis (‘‘nameko’’,

Usenko 1984). During exceptionally cold winters, the shoot

tips, even on mature trees, may be injured in the north part

of the natural range.

Biochemical peculiarities of Mandshurian ash

Due to its significant external resemblance to Black ash (F.

nigra), Mandshurian ash has been even considered to be a

black ash variety, F. nigra var. mandshurica (Rupr.) Lin-

gelsheim. However, the chemical compounds in Mand-

shurian ash phloem are unique and toxic or deterrent to

herbivores (Whitehill et al. 2012). In particular hydrox-

ycoumarins and the phenylethanoids, calceloariosides A

and B have been considered to be compounds that possibly

determine the resistance of this species against emerald ash

borer, Agrilus planipennis (Eyles et al. 2007). Clear dif-

ferences between Mandshurian ash and North American

ash species were revealed in relation to this ash borer,

Mandshurian ash also being characterized by a rapid rate of

wound browning, high soluble protein concentration and

low trypsin inhibitor activity, acting as chemical defences

(Cipollini et al. 2011).

A. planipennis has been accidentally imported from Asia

to North America, where this borer, discovered in 2002,

has killed millions of trees of indigenous ash species and

became one of the most destructive forest pests in North

America (MacFarlane and Meyer 2005; Poland and

McCullough 2006; Eyles et al. 2007; Siegert et al. 2010). A

year later, in 2003, this borer was first discovered in

Moscow, Russia, and by today it has occupied a territory of

150,000 km2 (Orlova-Benkovskaya 2013). Although we

could not find in the literature any indications that the

Eur J Forest Res

123

importation of A. planipennis to America or to Eastern

Europe has been attributed to the introduction of Mand-

shurian ash, a parallel with the possible introduction of H.

pseudoalbidus through Mandshurian ash to Europe at

almost the same time seems to be noteworthy.

Out of its natural range: Mandshurian ash

as an introduced species

For a long period, mainly historical obstacles have hin-

dered the introduction of East Asian plants to Europe and

North America. The Russians were the first to distribute

them (Koponen and Koponen 1995), as we saw before—

actually together with or by Baltic Germans.

At the location closest to Estonia, where F. mandshurica

has been planted and investigated for a long time, St.

Petersburg (meanwhile: Leningrad, cf. Fig. 1, point 1),

nearly all Russian Far East tree species have been approved

for introduction in non-native areas, several of them for

repeated generations (Andronov 1953).

Extensive introduction of exotic tree species growing

naturally in the Far East to the western regions of the

Russian empire started in the middle of the nineteenth

century, after the journey of Richard Maack to these areas

(Plotnikova 1971). For the first time, F. mandshurica was

planted in the Botanical Garden of St. Petersburg in 1861,

only a few years after the first scientific description of it

(Ruprecht 1857) as a new species. Apparently, Richard

Maack brought the seeds from Far East himself. The suc-

cess during the first decades of its cultivation there is

unclear: in the beginning, this species was not considered

to be sufficiently cold resistant. E.R. [Eduard Regel?] has

written: ‘‘Im Amurland von Maximowicz entdeckt und

durch den Petersburger Garten eingefuhrt. Noch in

Petersburg hart’’ (CS 1879).

F. mandshurica was registered in St. Petersburg in

1861–1879, 1891–1898 and 1935–2005 (http://flower.

onego.ru/kustar/fraxinus.html). The first generation of F.

mandshurica in St. Petersburg was judged to be compara-

tively cold resistant (but only for good natural conditions)

or even less resistant (suitable, however, for cultivation in

the St. Petersburg region). However, during its second

generation, F. mandshurica proved to be totally frost

hardy, a result of evaluation after its acceptable survival

rate following the extremely cold winter of 1939–1940

(Andronov 1953). Recently, in November 2013, a trial to

find alive Mandshurian ash trees in the Botanical garden of

St. Petersburg, where this species was first planted in

Europe, ended with failure (R. Drenkhan, not published).

On the other hand, in the area where Mandshurian ash

(F. mandshurica) has been planted out of its range but

geographically closest to its natural range, i.e. in western

Siberia, this species has been classified as totally cold

resistant (Krylov 1950). In Krasnoyarsk city (Fig. 1, point

4), the height of trees (H) reached 9.3 m and the diameter

(DBH) 18 cm (at a non-specified age (!), Protopopova

1964).

The inventory of F. mandshurica trees introduced in

1936 from Habarovsk to the Middle Taiga subzone (Komi,

near Syktyvkar, Fig. 1, point 2) demonstrated that at the

age of 40 years, after the severe winter of 1978–1979, all

trees had died out (Martynov 2011). However, thereafter

the new accession of F. mandshurica trees was found to

grow in good condition, flowering and fruiting annually,

and has already yielded seeds to produce the next genera-

tion. At the age of 30 years, these trees reached H = 6.8 m

(Martynov 2011). Obviously for the fate of the first

accession, the last paper contains no conclusions regarding

the cold resistance of this species in Komi.

In the very dry summers and severely cold winters of

Central Asia (Kazakhstan, Uzbekistan and Turkmenistan,

Fig. 1, points 5, 6 and 7, respectively), introduced F.

mandshurica trees were judged to be entirely cold- and

heat resistant, and, additionally, relatively drought tolerant,

though appropriate only for ornamental purposes (Schipt-

scinski 1953), whereas European ash (F. excelsior) in the

harsh areas of central Kazakhstan has been evaluated as

unsuitable (Rubanik 1980).

Introduced to Moscow (Fig. 1, point 3), at the age of

10 years, the height of F. mandshurica trees outperformed

even the growth of this species in its natural range (Plot-

nikova 1971).

In the southern part of the province of Livland of the

Russian empire (modern Latvia), F. mandshurica was first

mentioned in the Wagners’ tree nursery close to Riga

(Wagner 1877). The origin of the Mandshurian ash’s

planting stock there remains unknown; the seeds might

have originated in St. Petersburg. Recently, in 2008, F.

mandshurica was registered in eight different localities in

Latvia (Laivins et al. 2008, see Fig. 4).

In Finland, a few individual trees of F. mandshurica are

growing only in the southernmost part of the country

(Fig. 4). However, given that the cold resistance of the

species there is considered to be higher than that of F.

excelsior (http://www.mustila.fi/taxonomy/term/167, see:

UKK: 21), it is evaluated as a promising species for

expanding the range of ash trees northward. The area of

origin of F. mandshurica trees introduced to Mustila

arboretum is in Birobidzhan (Russian Far East, 48�300N,

133�000E) (Ulsike 1992), i.e. in the north-western region of

its natural range (Fig. 3, dendrofloristic area 25). In 1993, a

consignment of F. mandshurica var. japonica seeds was

brought to Finland from Hokkaido (Koponen and Koponen

1995). Since we could not find any registered cases of

introduction of F. mandshurica var. japonica to Estonia,

Eur J Forest Res

123

the closest point of growing of this definite variety of host

plant species for H. pseudoalbidus to our area is situated in

Helsinki (in Kaisaniemi and Kumpula arboreta, Leo Juni-

kka, pers. comm.), i.e. ca 100 km from the nearest area of

northernmost Estonian stands of F. excelsior.

The history of introduction of Mandshurian ash

to Estonia

In Estonia, F. mandshurica is still planted only in small

numbers and can be found mostly as individual trees. The

tree is considered to be rather cold resistant and—due to

the lower growth rate compared with European ash (F.

excelsior)—recommended mostly for the western islands

with milder climate. However, young F. mandshurica trees

may suffer from late frosts (Laas 1987).

Pre-Soviet introductions

According to Dietrich (1865), F. mandshurica was already

cultivated in the territory of present-day Estonia in the

early 1860s, i.e. the decade after its first scientific

description. The first locations of F. mandshurica were

documented in Tallinn (Fig. 4, point 1). The provenances

of these trees were described as Mandshuria and Amur

(Dietrich 1865). It is also possible that a well-known Baltic

German naturalist, Carl von Ditmar, brought F. mandshu-

rica seeds personally from his expedition to the Amurland

in 1855–1856, apparently accompanying Richard Maack.

He was the owner of Karu (Kerro) Manorial estate in Rapla

county (central part of north-western Estonia, ref.

Tammiksaar 2011). Tree nursery owner in Tallinn H.A.

Dietrich could also have obtained F. mandshurica seeds

or plants from the botanical gardens of the universities of

St. Petersburg or Tartu (Dorpat). However, the latter is

questionable since F. mandshurica was not mentioned in

the Botanical garden of Tartu University at the second

half of the nineteenth century (e.g. Willkomm 1873;

Klinge 1883).

The oldest deposited Estonian (sampled namely in

Tartu) exemplar of F. mandshurica in the herbarium of the

vascular plants of Tartu (Dorpat) University originates

from 1877 (Kaili Orav, pers. comm.), which demonstrates,

however, that at the time of the shown above inventories of

Willkomm (1873) and Klinge (1883), this species had to

grow in Tartu. At 1883, J. Klinge characterized the

occurrence of F. mandshurica in Estonia as follows:

‘‘Seltener, bei Reval hafiger, angepflanzt. Sceint vollig hart

zu sein’’, i.e. uncommon/in Estonia/, frequent in Reval/i.e.

in Tallinn/,/cold/resistant (Klinge 1883). It is possible,

however, that Klinge got these data from the paper of

Dietrich (1865) or from Dietrich personally.

The next introducer of F. mandshurica seeds or plants to

Estonia, and the first, who certainly imported them directly

from the native range of F. mandscurica in the Russian Far

East, was count Friedrich Georg Magnus von Berg, owner

of the Sangaste Manorial estate (southern Estonia, Fig. 4,

point 2). In 1903, he made an extensive journey to the far

eastern lands of Russia (Berg-Sagnitz 1904; Kasesalu

1995). In the list of tree species of his manorial estate, the

species of interest here was registered twice, in 1923 and

1926 (Berg 1924; Sander 2000). A more exact origin of

these seeds from inside the natural range of Mandshurian

ash in the Russian Far East remains unknown.

Fig. 4 Registered habitats of

introduced Mandshurian ash (F.

mandshurica) in Estonia

(?Latvia and southern Finland):

grey pricks on the map of

Estonia indicate the areas with

higher abundance of European

ash (F. excelsior), filled rings—

definite (registered by

experienced dendrologists)

Mandshurian ash tree growing

points, most important of which

are numbered (1—Tallinn, 2—

Sangaste, 3—Luua and 4—

Jarvselja). Mandshurian ash

habitats in Finland and Latvia

are mapped, according to the

sources: Koponen and Koponen

(1995), Leo Junikka (pers.

comm.) and Laivins et al.

(2008)

Eur J Forest Res

123

Directly before the Soviet occupation, in the list of

planting stock of trees and shrubs proposed for sale in the

forest enterprises of Estonia, 20 seedlings of F. mandscu-

rica were offered only in Ahja (south Estonia), of an

unknown origin (Vilbaste 1939).

Introductions during the Soviet occupation period

In 1948, a consignment of F. mandshurica seeds was

brought from Leningrad (St. Petersburg) to the Luua

(Fig. 4, point 3). Some seedlings were grown in the nursery

and planted in 1953–1954 at the local arboretum. Soon

these plants were affected by late frosts (Ilves 2002). A

number of these plants (in total 105) also could have

originated from the botanic garden of Moscow University.

Several surviving seedlings were distributed to other places

of Estonia. Their fate is unknown. By 1973 only seven

Mandshurian ash trees had survived in Luua and by 2011

only one, definitely originating from Moscow (I. Kandima,

pers. comm.).

In 1950, a report, based on the investigations of the

exotic tree species in Estonia from 1930 to 1948, was

compiled (Michelson 1950). F. mandscurica was found

there to grow only in Sangaste and in Jarvselja (Fig. 4,

points 2 and 4).

A known introduction of F. mandshcurica from its

natural range occurred in 1961, when A. Paivel brought

seeds from several localities in the Russian Far East. Of

these trees, only three individuals have survived in Tallinn.

They originate, respectively, from Aljochino and Okeans-

kaya (Fig. 3, area 33), and to document this consignment, a

herbarium list has been kept in the Tallinn Botanical

Garden (TALL A003188). The surviving trees, in general,

have not suffered from winter frosts, but during the low

snowfall winter of 2002/2003, after an extremely short

hardening period during the autumn of 2002 in Estonia

(Hanso and Drenkhan 2007), and after the winter of 2005,

some branches were affected. Before and after these severe

winters, the trees were evaluated as healthy (Paivel 1996;

O. Abner, pers. comm.). In 2010, these trees flowered and

their seeds (definite origin: Okeanskaya, 1961) were

available from the Tallinn Botanic Garden (Index seminum

2011).

During the 1970s, F. mandscurica seeds were brought

from Rikorda Island (Fig. 3, area 33) to Jarvselja (Fig. 4,

point 4); thereafter, this species was recorded in 1985 and

1995. Nursery stock was grown from these seeds and dis-

tributed (Sander 2012; Kasesalu, pers. comm.).

In 1975, live plants of F. mandscurica were brought to

the Tallinn Botanic Garden from the Bolshechichzir Nature

Reserve (south of Habarovsk city, Fig. 3, area 29). Up to

this point, only three individuals have survived; the same

harsh 2002/2003 winter damaged branches, but afterwards

the trees were judged as healthy. None of these trees have

flowered up today (Olev Abner, pers. comm.).

In 1977, F. mandscurica was brought to Estonia, as

seeds or as living plants, from the Nelma settlement, Pri-

morye, in the Russian Far East (Fig. 3, area 16). Origi-

nating from that planting stock, five trees were registered in

1996 (with the Hmax = 8.7 m, cf. Elliku and Sander 1996),

but by today only one tree has survived.

It is known that in 1985, a consignment of F. mand-

shurica was planted in the Kuremae arboretum (eastern

Estonia). The plants were grown from seeds brought from

Shamora (nearby to the city of Vladivostok, Fig. 3, area

33) by J. Elliku, who participated in 1981 in an expedition

to the Russian Far East. In 1999, only a single living tree

was registered there (Abner et al. 2004).

Definite points of origin in the natural range

of Mandshurian ash at the introductions to Estonia

The settlements in the Russian Far East, representing the

known areas of origin of F. mandscurica during its intro-

ductions to Estonia from the 1960s to the 1980s: Alyohino

(Kunashir Island, near the cape Stolbchatyi, introduction

year 1961), Okeanskaya (43�140N, 132�00E; 19 km north

of Vladivostok, on the bank of the Amur River, introduc-

tion year 1961), Bolshechichzir Nature Reserve Area, close

to Habarovsk, introduction year 1975), Nelma (47�390N,

139�100E; Primorye krai, Russko-gavanskiy region),

introduction year 1977), Shamora (18 km from Vladivo-

stok, introduction year 1981) and Rikorda island (south

from Vladivostok, introduction in the 1970s).

Known places in Estonia where Mandshurian ash

has been registered during the dendrofloristic revisions

in the middle and at the end of twentieth century

During the dendrological inspection of exotic tree species

in the middle of the twentieth century, F. mandshurica was

documented in the following arboretums and parks of Es-

tonia (Paivel 1996; Paivel and Sander 2004, deposited

herbarium lists are indicated as Tall A and serial number):

J. Alas (1954 and 1962); Tihemetsa (1954); Luua (1957

and 1963; Tall A003197); Kaagjarve (1960, Tall

A003196); Jarvselja (1961 and 1962; Tall A003193);

Tallinn (TBA, 1961); Poltsamaa (1961, Tall A003194), M.

Ranna (1962, 1964; Tall A003190); Mustvee (1962, Tall

A003191); and Jogeva (1962, Tall A003192). Definite

origins of Mandshurian ash trees listed above were not

specified, but obviously all were grown in Estonian forest

nurseries from the seeds or plants consignments, discussed

Eur J Forest Res

123

above. Some ash trees in Jarvselja were already planted

before 1940 (Kasesalu, pers. comm.).

During the dendrological inspection of exotic tree spe-

cies in the latter part of the twentieth century, F. mand-

shurica was documented in the following arboretums and

parks of Estonia, indicated in Fig. 4 (Laas 1994; Paivel

1996; Abner et al. 2004; Elliku and Sander 1999, 2004;

Sander 2012; Konnu dendropark 2007; Index seminum

2011; Kasesalu et al. pers. comm.): Parnu (1979, 1984 and

1986); Lasva (Voru, 1986); Villevere (Kabala 1987, 1991,

1998 and 2010, A. Ristkok, pers. comm.); Luua (1989 and

2011 I. Kandima, pers. comm.); Jarvselja (Agali, 1985,

1995 and Rokka 1995); Paasiku-Matsi (Schmeidt 1991);

Volumae (U. Sinisalu, Ragavere 1994 and 2000); Tartu

(Metsamaja, 1994); Pataste (A. Aadusoo, 1995); Kuremae

(A. Kurg, 1995 and 1999); Moisakula (Sorve, Saaremaa, A.

Ilus, 1995); Tallinn (TBA, 1996, origin: Okeanskaya, 1961

and M. Laane, 1997, origin: TBA, not surviving to 2013));

Rae (H. Karis, 5 trees in 1996, today only one alive tree);

and Neemi (M. Rand, Saaremaa, 1996); Konnu (Johvi, Il-

luka, 2001). By 2013, no more F. mandshurica trees were

found in Sangaste (R. Drenkhan, pers. comm.).

The death or disease in F. mandshurica trees referred to

above, in Estonia or in other referred areas, was related

solely to cold damage or had no known cause.

European ash (Fraxinus excelsior L.)

European ash and the disease initiation and progression

in Estonia

European ash (F. excelsior) belongs to the scattered

broadleaved tree species in Europe, due to its scattered

distribution in mixed forests and requirements for specific

site and habitat conditions (Dobrowolska et al. 2011). Sites

for growing European ash have been predicted to become

more abundant at the northern limit of its natural range

(Hemery et al. 2010), consequently incl. Estonia: The

northern border of the natural range of European ash at the

geographical longitudes of the Baltic countries lies at the

southernmost Finland (Hamet-Ahti et al. 1992), close to

Estonia. In Estonia, pure European ash stands are rare (only

ca 0.1 % of the total forested area). The abundance of

European ash in mixed stands decreases from northwest to

the southeast (Fig. 4), as the climate becomes increasingly

continental. Natural regeneration is the predominant way of

European ash regeneration (Valk and Eilart 1974). How-

ever, the European ash is popular as an ornamental tree,

occurring as single trees or small groups in many parks

across Estonia (Kuusk et al. 1996).

Vague health problems in European ash trees of differ-

ent ages were first noticed in the Aamse Nature Reserve

area (northwest Estonia, 58�560N, 23�420E) in 1995, i.e. in

the region with more frequent ash occurrence (Fig. 4), and

in 2001 in Hiiumaa (Dago) Island (Ploompuu 2007). As

can be seen from the figure, the first disease incidences

were not associated with areas where Mandshurian ash had

been planted. By 2003, the disease had reached essentially

most of ash stands in north-western Estonia. Reports about

this reached the authors of this paper simultaneously in

2003. Immediate pathological inspection of several ash

trees and stands of different ages in central and south-

eastern Estonia did not reveal any suspicious phenomena.

These areas became visibly infected with the disease only

in 2006–2007, and by 2008, the country was totally colo-

nized (Drenkhan and Hanso 2009). As definite losses, for

instance, from 2009 to 2013, about half of the ash trees

growing in overstorey and subcanopy layers were killed in

a productive forest of an isolated East-Estonian area

(Lohmus and Runnel 2014).

Up to this point, the appearance of ash stands in north-

western Estonia had improved somewhat, especially in the

youngest, naturally regenerated trees. Still, mainly older

trees were badly damaged, although 5–10 % of them

showed only mild damage (Ploompuu 2013). Really, Pliura

et al. (2011) have demonstrated in Lithuania that resistance

of F. excelsior against C. fraxinea is genetically deter-

mined and heritable.

Similar to the situation in Estonia (Drenkhan and Hanso

2009), the epidemic on F. excelsior was found to expand

from west to east in Finland (Rytkonen et al. 2011, Fig. 4),

where European ash is growing only in the southernmost

(particularly south-western) region of the country (Hamet-

Ahti et al. 1992). Apparently the disease started to dis-

seminate there eastward from the southwesternmost terri-

tory, i.e. from the Aland Archipelago, where the

symptomatic European ash trees were noticed much earlier

than in mainland Finland, i.e. since 2000 (Rytkonen et al.

2011).

Meeting of European ash with Mandshurian ash

and the release of epidemic

The first time when Chalara fraxinea (the teleomorph of H.

pseudoalbidus) on Mandshurian ash (F. mandshurica) was

documented in Europe occurred in Estonia (Drenkhan and

Hanso 2010). As demonstrated above, Mandshurian ash

has grown in Estonia for nearly 150 years, but large-scale

emergence of the dieback on the indigenous European ash

began only ca 1–1.5 decades ago. Whether or not signifi-

cant events that increased the disease vulnerability have

occurred earlier with the pathogen (H. pseudoalbidus) or

with the new host (F. excelsior) in its ancient home, i.e. in

Europe, is still not known. It is worth noting that simul-

taneously with the emergence in 1990s of the very first

Eur J Forest Res

123

dieback symptoms on European ash trees in the Baltic

countries and eastern Poland, now attributed to C. fraxinea,

the health problems on European ash (forking of shoots,

etc.), not addressed to C. fraxinea, started in southern

Britain (Kerr and Boswell 2001). C. fraxinea was not

reported in southern Britain before 2012 (Anonymous

2012). Similarly, in recent decades, the health problems

(twig and branch dieback, epicormic branching and thin-

ning of crowns) of unknown aetiology were registered in

Black ash (F. nigra) throughout its natural range in North

America (Palik et al. 2012). In Turkey, nearly all the

investigated F. ornus trees were found to have health

problems, a fourth of them bearing dry shoots (Lehtijarvi

et al. 2009). Could there be a worldwide general stress of

still unknown aetiology on ash trees as a pre-requisite for

the epidemic (in Europe) and calamity (in North America

and Eastern Europe), and is it time when the applied

research should turn more to the ecological and patho-

physiological investigations of the host trees? Noteworthy

is also that H. pseudoalbidus has caused some damage,

although low scale, to F. mandshurica in Estonia (Drenk-

han and Hanso 2010), but not in Japan (Zhao et al. 2012)

nor in China (Zheng and Zhuang 2013). However, we

cannot exclude from here also the possible additional role

of pure suitability of some provenances of F. mandshurica

to Estonia, as it had repeatedly come out also in the long-

lasting experience of introduction.

Considering the crossing entire Eurasia arc-shaped belt,

formed by the natural ranges of more than 20 different ash

species (Krussmann 1965) and the biogeographical history

of the genus Fraxinus on this continent (Hinsinger et al.

2013), there is also a theoretical possibility of the arrival of

H. pseudoalbidus from Far East to Europe alongside that

belt. As it passes dry and warm Central Asia, we included

to this review also information about the behaviour of

Mandshurian ash as an introduced species in Kazakhstan,

Uzbekistan and Turkmenistan (see before).

European ash in the natural range of Mandshurian ash?

Our search in the literature sources which could report (in

English or in Russian) any opposite direction introductions,

that is, introductions of F. excelsior to the natural range of

F. mandshurica, unfortunately ended without results,

except of a single reference—an Erysiphaceous fungus

(Uncinula fraxini) has been described definitely on leaves

of European ash (F. excelsior) in the Ussuuri Botanic

garden in Primorye (Azbukina 1991). Our recent enquiry

there remained not answered. Cultivation experiments of F.

excelsior in Japan, especially at the last decades, i.e. at the

time of the first record of Lambertella albida (=H.

pseudoalbidus) in Hokkaido, Japan, cf. Hosoya et al.

(1993), might betray the approximate emergence time of

the virulence in H. pseudoalbidus. Why did the disease

emerge in Estonia just recently and not a century ago?

Generally, the first records and scientific investigations of

fungal species coincide with abrupt changes in their

behaviour, abundance, or other characteristics, and scien-

tific information regarding behaviour of F. excelsior in East

Asia would be essential for clearing up the time of possible

changes in the fungus—if the question lies solely in the

fungus.

Uni-, bi- or pluricentric emergence?

Even the possibility of pluricentric emergence of the

European ash dieback in Europe may be taken into con-

sideration in locating the invasion routes and pathways of

H. pseudoalbidus. High genetic diversity or high number of

different alleles in a population may suggest not only an

early occurrence of a fungus in a site, but may also cite to

several introductions. Really, based on RAMS finger-

printing, the H. pseudoalbidus population study in Estonia

and Finland (Rytkonen et al. 2011) revealed considerable

genetic variation. However, a large genetic variation of H.

pseudoalbidus was recorded also in Poland (Kraj and Ko-

walski 2013) and in other different European countries

(Bengtsson et al. 2012), apparently less often settled by

Mandshurian ash from its natural range than it occurred in

Estonia. However, much more information is needed for

posing a bi- or even pluricentric hypothesis to the emer-

gence of the epidemic in Europe. If to consider the more

than a century-long introduction history of Mandshurian

ash to Estonia, then namely here another epicentre could

find place. The epicentre of emergence and the direction of

progression of the epidemic in Estonia and Finland, not

supporting the unicentric hypothesis in Europe, might be

the first arguments for posing an appropriate hypothesis.

Also the possibility of a different and fast way of dis-

semination of the pathogen—entomochorous (e.g. Trans-

Baltic, via Gotland and Aland Archipelago) dispersal—

should not be ignored. However, during the last decades,

no remarkable migration of alien or native for North Eur-

ope ash insects along or over the Baltic Sea has been

registered (Ilmar Suda and Erki Ounap, pers. comm.-s).

Similarly unknown are any movements of planting stock of

European ash from Poland or Lithuania to Estonia during

the last decade of the twentieth century and after, which

could pose an alternative pathway to the arrival of the

pathogen from the hypothetical single centre.

Acknowledgments Prof. Ottmar Holdenrieder (Institute of Inte-

grative Biology, Zurich, Switzerland) and Dr. Ari Hietala (Norwegian

Forest and Landscape Institute, As, Norway), serving as pre-sub-

mission reviewers, and three unknown reviewers are highly appreci-

ated for their valuable comments and suggestions. We thank several

dendrologists (cited in the text) for their personal communications,

Eur J Forest Res

123

enriching this paper with the up-to-date information about the state of

introduced Mandshurian ash trees in Estonia (and in Finland and

Latvia). Mr. Terry Bush (Madison, Wisconsin, USA) is appreciated

for the language revision. This project was supported by the Estonian

Environmental Investments Centre and the Institutional Research

Funding IUT21-04.

References

Abner O, Elliku J, Sander H (2004) Survey of fifteen larger private

collections. Researches of woody plants of Estonia. VIII.

Overview of tree plants of arboretums and parks. Tallinn, OU

Infotrukk, pp 93–194 (in Est)

Andronov NM (1953) About the winter-resistance of trees and shrubs

in Leningrad. In: Sokolov, SY (ed) Introduction of plants and

creation of verdant areas, ser 6, 3rd edn. Works of the Botanical

Institute VL Komarov Acad Scienc USSR, pp 165–220 (in Russ)

Anonymous (2012) Chalara fraxinea in ash trees in Great Britain.

Forestry Commission Bulletin (England), October 2012. http://

www.forestry.gov.uk/pdf/Email-Alert-121001.pdf/$FILE/Email-

Alert-121001.pdf

Azbukina ZM (chief editor) (1991) Lower plants, fungi and mosses of

the Soviet Far East. Fungi, Part 2, Ascomycetes. Leningrad,

Nauka, p 123 (in Russ)

Bengtsson SBK, Vasaitis R, Kirisits T, Solheim H, Stenlid J (2012)

Population structure of Hymenoscyphus pseudoalbidus and its

genetic relationship to Hymenoscyphus albidus. Fungal Ecol

5(2):147–153

Berg F (1924) Tree orders in the forest and park of Sangaste. Est

Forest 17(18):177–180 (in Est)

Berg-Sagnitz F (1904) Vom Baltischen Meer zum Stillen Ocean.

1803. Riga, Gedr Mullershen Buchdruck, 217 S

Britton KO, Liebhold AM (2013) One world, many pathogens! New

Phytol 197:9–10

Cipollini D, Wang Q, Whitehill GA, Powell JR, Bonello P, Herms

DA (2011) Distinguishing defensive characteristics in the

phloem of ash species resistant and susceptible to Emerald ash

borer. J Chem Ecol 37:450–459

Cleary MR, Arhipova N, Gaitnieks T, Stenlid J, Vasaitis R (2013)

Natural infection of Fraxinus excelsior seeds by Chalara

fraxinea. For Pathol 43:83–85

CS (1879) Bemerkungen uber verschiedene altere und neuere

Freilandgeholze. Gartenflora. Bd. 28:10–16 http://www.biodiver

sitylibrary.org/item/123931#page/25/mode/1up

Dietrich HA (1865) Alphabetisch Geordnetes Verzeichnib der

Zierbaume und Straucher Welche in der Garte der Provinz

Ehstland etc. Mitteilungen uber die Wirsksamkeit der Ehstlan-

dischen Gartenbau-Vereins zu Reval. Reval 2:12–35

Dobrowolska D, Hein S, Oosterbaan A, Wagner S, Clark J,

Skovsgaard JP (2011) A review of Europeana ash (Fraxinus

excelsior L.): implications for silviculture. Forestry 84:133–148

Drenkhan R, Hanso M (2009) Decline of European ash in Estonia and

elsewhere in Europe. Est Nat 60(3):14–19 (In Est)

Drenkhan R, Hanso M (2010) New host species for Chalara fraxinea.

New Dis Rep 22:16

Elliku J, Sander H (1996) A commented list of tree plants of the Rae

arboretum in Harju county. In: Eensaar A, Sander R (eds)

Human influence to the environment of Tallinn III, Tallinn,

pp 270–278 (in Est)

Elliku J, Sander H (1999) An overview of nine arboreta and

dendrogardens of Parnu county. Research of woody plants of

Estonia IV Tallinn, pp 9–74 (in Est, lists in Latin and Est)

Elliku J, Sander H (2004) Collections of woody plants of Mati Laane

and Peeter Viikholm in Tallinn. Research of woody plants of

Estonia VIII Tallinn, Overview of woody plants in arboreta and

parks. OU Infotrukk, pp 195–221 (in Est)

Eyles A, Jones W, Riedl K, Cipollini D, Schwartz S, Chan K, Herms

DA, Bonello P (2007) Comparative phloem chemistry of

Mandshurian ash (Fraxinus mandshurica) and two North

American ash species (Fraxinus americana and Fraxinus

pennsylvanica). J Chem Ecol 33:1430–1448

Gross A, Holdenrieder O, Pautasso M, Queloz V, Sieber TN (2014)

Hymenoscyphus pseudoalbidus, the causal agent of European ash

dieback. Pathogen profile. Mol Plant Pathol 15:5–21

Hamet-Ahti L, Ahti T, Koponen T (1974) A scheme of vegetation

zones for Japan and adjacent regions. Ann Bot Fenn 11:59–88

Hamet-Ahti L, Palmen A, Alanko P, Tigerstedt PMA (1992) Finnish

flora of trees and shrubs/. Helsinki, Dendrol Seura (in Finn)

Hanso M, Drenkhan R (2007) Forest and town trees are suffering

from the extreme weather conditions. Est Nat 58:6–13 (In Est)

Harvard University Herbaria Barcode GH00073884. Fraxinus mand-

shurica Ruprecht. Index of Botanical Specimens. http://kiki.huh.

harvard.edu/databases/specimen_search.php?mode=details&id=

43317

Hemery GE, Clark JR, Aldinger E, Claessens H, Malvolti ME,

O‘Connor E, Raftoyannis Y, Savill PS, Brus R (2010) Growing

scattered broadleaved tree species in Europe in a changing

climate: a review of risks and opportunities. Forestry 83(1):

65–81

Hinsinger DD, Basak J, Gaudeul M, Cruaud C, Bertolino P, Frascaria-

Lacoste N, Bousquet J (2013) The phylogeny and biogeographic

history of ashes (Fraxinus, Oleaceae) highlight the roles of

migration and vicariance in the diversification of temperate trees.

PLoS One 8(11):1–14

Hosoya T, Otani Y, Furuya K (1993) Materials for the fungus flora of

Japan (46). Trans Mycol Soc Jpn 34:429–432

http://mustila.fi/taxonomy/term/167, see: UKK: 21

http://flower.onego.ru/kustar/fraxinus.html Ash in the Botanical Gar-

den of Sankt Petersburg. Encyclopedia of ornamental garden

plants

Hu L-J, Uchiyama K, Shen H-L, Saito Y, Tsuda Y, Ide Y (2008)

Nuclear DNA microsatellites reveal genetic variation but a lack

of phylogeographical structure in an endangered species, Frax-

inus mandshurica, across North-east China. Ann Bot 102:

195–205

Ilves E (2002) Luua arboretum—the most interesting dendrological

collection in Central Estonia. Dendrol Research Estonia/III,

Tallinn, pp 116–140 (in Est)

Index seminum (2011) anno 2010 collectorum quae Hortus Botanicus

Tallinensis pro mutual commutatione offert (2011) Tallinn

Juodvalkis A, Vasiliauskas A (2002) The extent and possible causes

of dieback of ash stands in Lithuania. LZUU Mokslo Darb.

Biomed Moksl 56:17–22 (in Lithuan)

Kasesalu H (1995) Count Friedrich Berg as introducer of exotic tree

species to Estonia. In: Paves H (ed) Count Friedrich Berg and

forest. TA Kirj, Tartu-Tallinn, pp 14–24 (In Est)

Kerr G, Boswell R (2001) The influence of spring frosts, ash bud

moth (Prays fraxinella) and site factors on forking of young ash

(Fraxinus excelsior) in southern Britain. Forestry 74:29–40

Kirisits T, Matlakova M, Mottinger-Kroupa S, Cech TL, Halmsch-

lager E (2009) The current situation of ash dieback caused by

Chalara fraxinea in Austria. In: SDU Facult Forestry Journal,

Ser: A, Special Issue, pp 97–119

Klinge J (1883) Die Holzgewachse von Est-, Liv- und Curland.

Verlag C Mattiesen, Dorpat, 290 S

Konnu Dendropark (2007) List of species. http://konnudendropark.

com/liikide-nimekiri/ (in Est and Latin)

Koponen T, Koponen A (1995) Expedition of the Botanical Garden,

University of Helsinki, to Northeast China. Sorbifolia

26:107–125 (in Finn)

Eur J Forest Res

123

Kowalski T, Łukomska A (2005) Studies of Fraxinus excelsior L.

dieback in stands of Wloszczowa Forest Unit. Acta Agrobot

59:429–440 (in Polish)

Kraj W, Kowalski T (2013) Genetic variability of Hymenoscyphus

pseudoalbidus on ash leaf rachises in leaf litter of forest stands in

Poland. J Phytopathol 162(4):218–227

Krestov PV (2003) Forest vegetation of Easternmost Russia (Russian

Far East). In: Kolbek J, Srutek M, Box EO (eds) Forest

vegetation of Northeast Asia. Kluwer, Dordredcht, pp 93–180

Krussmann G (1965) Die Laubgeholze. Eine Dendrologie fur die

Praxis. Paul Parey, Berlin u. Hamburg, 389 S

Krylov GV (1950) Cold resistance of trees introduced to the forest

nursery of the Botanical garden of the Western Siberian branch

of the USSR Academy of Sciences. Bull Centr Bot Garden 6 (in

Russ)

Kuusk V, Tabaka L, Jankeviciene (eds) (1996) Flora of the Baltic

countries. II. Estonian Acad Sciences. Instit Zool Bot, Latvian

Acad Sciences, Instit Biol, Lithuanian Inst Bot. Eesti Loodusfoto

AS, Tartu

Laas E (1987) Dendroloogia / Dendrology/. Tallinn, Valgus (in Est)

Laas E (1994) 20 years of Dendrological park of the Faculty of

forestry of the Estonian University of Life Siences. Est For

22:5–9 (In Est)

Laivins M, Bice M, Krampis I, Knape D, Smite D, Sulcs V (2008)

Latvijas Kokaugu atlants/Atlas of Latvian woody plants/. Latv

Universit, Biol Inst, Rıga (in Latv)

Lehtijarvi A, Dogmus-Lehtijarvi HT, Karadeniz M, Uygun M (2009)

Dieback on Fraxinus ornus in Konya region. SDU Facult For J,

Ser A, Special Issue, pp 120–128

Liu H, Zhu H, Guo C, Xia D (1997) Study on the provenance of

Fraxinus mandshurica. J For Res 8(1):10–12

Lohmus A, Runnel K (2014) Ash dieback can rapidly eradicate

isolated epiphyte populations in production forests: a case study.

Biol Conserv 169:185–188

MacFarlane DW, Meyer SP (2005) Characteristics and distribution of

potential ash tree hosts for emerald ash borer. For Ecol Manag

213:15–24

Martynov LG (2011) Introduction of Far Eastern woody plants to the

Middle-Taiga subzone of the Komi Republik. Contempor Prob

Ecol 4(3):260–265

Maximovicz C J (1875) Diagnoses des nouvelles plantes du Japan et

de la Mandjourie. XIX decade. Bull Cl Phys-Math Acad Imp Sci

St-Petersbourg-Tome 20:430–472. http://www.biodiversityli

brary.org/item/27835#page/242/mode/1up

Michelson A (1950) Cultivation of exotic tree species in Estonia.

Tartu. (Manuscr, Inst Forestry and Rural Engin, Estonian Univ

Life Scienc, Tartu, Estonia) (in Est)

Nedolushko VA (1995) Outline of the dendroflora of the Russian Far

East. Vladivastok, Dalnauka (in Rus) (cf. Petropavlovskiy et al.

2011)

Ogureeva GN, Dudov SV, Karimova TYu (2012) Ecosystem diversity

and protection of Korean pine-broadleaved forest. Broadleaved

of the Manshurian natural area. Lesoved/Forestry/2: 47–60 (in

Russ, abstr in Eng)

Orlova-Benkovskaya MJ (2013) Emerald ash borer (Agrilus

planipennis) has been distributed into nine regions of the

European Russia: from Yaroslavl until Voronez. In: VII

Readings in Memory of O.A. Katayev. Materials of an

international conference, Sankt-Peterburg, 25–27 November,

2013, pp 65–66

Paivel A (ed) (1996) Index plantarum. Catalogue of plant collections.

Tallinn Bot Garden, RAS Bit, Tallinn

Paivel A, Sander H (2004) Tree plants of the most rich-in-species

collections at 1954–1968. Research of woody plants of Estonia.VIII. Tallinn, Overview of woody plants in arboreta and parks.

OU Infotrukk, pp 53–92 (in Est)

Palik BJ, Ostry ME, Venette RC, Abdela E (2012) Tree regeneration

in Black ash (Fraxinus nigra) stands exhibiting crown dieback.

For Ecol Manag 269:26–30

Pautasso M, Aas G, Queloz V, Holdenrieder O (2013) European ash

(Fraxinus excelsior) dieback—a conservation biology challenge.

Biol Conserv 158:37–49

Petropavlovskiy BS, Urusov VM, Brishataya AA (2011) Distribution

of life-forms of Russian Far East dendroflora in relation to the

warmth provision and oceanic influence. Ecol 2:97–101 (in Russ,

abstr in Eng)

Pliura A, Lygis V, Suchockas V, Bartkevicius E (2011) Performance

of twenty four European Fraxinus excelsior populations in three

Lithuanian progeny trials with a special emphasis on resistance

to Chalara fraxinea. Baltic For 17:17–33

Ploompuu T (2007) Farewell, Estonian ash stands! Est Nat 58:14–15

(In Est)

Ploompuu T (2013) Ash dieback and ash forests. Est Nat 64:54–55 (In

Est)

Plotnikova LS (1971) Introduction of woody plants of the Chinese-

Japanese floristic subregion to the Moscow. Moscow, Nauka,

135 (in Russ)

Poland TM, McCullough DG (2006) Emerald ash borer: Invasion of

the urban forest and the threat to North Americas ash resource.

J For 104(3):118–124

Protopopova EN (1964) Exotics/trees/in the Southern part of the

Krasnoyarsk region. In: Selection of tree species in the Eastern

Sibiria. Acad Scienc USSR, Siberian Department, Inst Forest

and Wood, pp 69–79 (in Russ)

Przybył K (2002) Fungi associated with necrotic apical parts of

Fraxinus excelsior shoots. For Pathol 32:387–394

Queloz V, Grunig CR, Berndt R, Kowalski T, Sieber TN, Holden-

rieder O (2011) Cryptic speciation in Hymenoscyphus albidus.

For Pathol 41:133–142

Rubanik VG (1980) Introduction of European trees and shrubs in

Kasakhstan. Alma-Ata, Nauka, 192 (in Russ)

Ruprecht FJ (1857) Die ersten botanischen Nachrichten uber das

Amurland. Zweite Abteilung. Baume und Straucher, beobachtet

von Richard Maack, bestimmt von F. J. Ruprecht. (Lu le 16

janvier 1857). (Schluss)—Bull. Cl. Phys.-Math. Acad. Imp. Sci.

Saint-Petersbourg 1857. 15(23). 24: 353–383. http://archive.org/

stream/bulletindelacla02naukgoog#page/n206/mode/1up

Rytkonen A, Lilja A, Drenkhan R, Gaitnieks T, Hantula J (2011) First

record of Chalara fraxinea in Finland and genetic variation

among isolates sampled from Aland, mainland Finland, Estonia

and Latvia. For Pathol 41:169–174

Sander H (2000) An overview of some works of Eduard Viirok.

Studies of woody plants in Estonia. Part V. Tallinn (in Est., abstr.

in Engl.)

Sander, H (comp.) (2012) The list of woody plants of the Jarvselja

teaching and experimental foundation (maintained in Jarvselja)

(in Estonian, List in Latin)

Schiptscinski NV (1953) Materials about the introduction of trees and

shrubs onto the plains of Central Asia. In: Sokolov SY (ed)

Introduction of plants and creation of verdant areas, Ser 6, 3rd

edn. Transact Bot Inst Komarov, pp 286–400 (in Russ)

Siegert NW, McCollough DG, Williams DW, Fraser I, Poland TM,

Pierce SJ (2010) Dispersal of Agrilus planipennis (Coleoptera:

Buprestidae) from discrete epicentres in two outlier sites.

Environ Entomol 39:253–265

Skuodiene L, Grybauskas K, Palionis V, Maslinskas R (2003) The

health condition of ash stands and possible reasons of their

dieback. Miskininkyste 54:86–96 (in Lithuan)

Su H-Y, Lin D-B (2003) Influence of main site factors on Fraxinus

mandshurica (Oleaceae) plantation. J For Res 14(1):83–86

Takhtajan A (1986) Floristic regions of the World. University

California Press, California

Eur J Forest Res

123

Tammiksaar E (2005) Maack Richard Otto. In: Nutfall, M. (ed.)

Encyclopedia of the Arctic. N Y & London: Routledge, Vol 2:

1217–1218

Tammiksaar E (2011) Carl von Ditmar—ein Geologe aus Livland in

russischen Diensten. In: Kasten E, Durr M (eds) Karl von

Ditmar. Reisen und Aufenthalt in Kamtschatka in den Jahren

1851–1855. Zweiter Teil. Allgemeines uber Kamtschatka. Nor-

dersted Verlag der Kulturstiftung Sibirien. SEC Publication,

pp 232–248

Thomsen IM, Skovsgaard JP, Kjær ED, Nielsen LR (2009) Status for

asketoptørre I Danmark og Europa. Skoven 2:87–91

Timmermann V, Børja I, Hietala AM, Kirisits T, Solheim H (2011)

Ash dieback: pathogen spread and diurnal patterns of ascospore

dispersal, with spezial emphasis on Norway. EPPO Bull 41:

14–20

Tomoshevich M, Kirichenko N, Holmes K, Kenis M (2013) Foliar

fungal pathogens of European woody plants in Siberia: an early

warning of potential threats? For Pathol. doi:10.1111/efp.12036

Ulsike (1992) 15. Fraxinus mandshurica—mantsuriansaarni. http://

www.mustila.fi/ulsike/FraxinusMandshurica (in Finn)

Usenko NV (1984) Trees, shrubs and lianas of Far East. Habarovsk

(in Russ)

Valk U, Eilart J (eds) (1974) Estonian forests. Valgus, Tallinn (in Est)

Vasiliauskas A, Juodvalkis A, Treigiene A (2002) Possible causes of a

massive dieback of ash in forests of Lithuania. In: Storozhenko

VG (ed) Proceedings of fifth international conference on forest

pathol and mycol. Russian Academic Science, Moscow,

pp 35–37 (in Russ)

Vasilyev VN (1952) Oleaceae. In: Shishkin BK, Bobrov EG (eds)

Flora USSR, XVIII. Editio Academ Scient USSR, Mosqua-

Leningrad, pp 483–525 (in Russ)

Vilbaste G (1939) Experiments with the acclimatisation of trees and

shrubs in the state forest enterprises. Est For 11:392–396 (in Est)

Viryasov BA (1933) Forests of the Far East region. Goslestehizdat,

Moscow (in Russ)

Wagner CH (1877) Illustrierter Katalog von Baumen, Strauchern,

Rosen, Stauden, Kalt- und Warmhousepflanzen, Gartengeratss-

chaften etc. von C.H. Wagner in Riga. 1877–1878. Gedr

Mullerschen Buchdruckerei, Riga, 127 S

Wang Y (1995) Study on ecology of Fraxinus mandshurica. J For Res

6(3):61–64

Wenzhang W, Jie C, Yulong F, Baoyou Z, Zhongyao J, Zhunhui Y

(1995) Study of physiological characteristics of Larix olgensis

and Fraxinus mandshurica under controlled conditions. J North-

east For Univ 6(1):1–5

Whitehill JGA, Opiyo O, Koch JL, Herms DA, Cipollini DF, Bonello P

(2012) Interspecific comparison of constitutive ash phloem phenolic

chemistry reveals compounds unique to Mandshurian ash, a species

resistant to Emerald ash borer. J Chem Ecol 38:499–511

Willkomm M (1873) Der botanische Garten der Kaiserlichen

Universitat Dorpat. Verl von C. Mattiesen, Dorpat, 179 S

Xiongwen C, Guangsheng Z, Zhang X (2002) Spatial characteristics

and change of forest tree species along the North East China

Transect (NECT). Plant Ecol 164:65–74

Yamamoto F, Sakata T, Terazawa K (1995) Physiological, morpho-

logical and anatomical responses of F. mandshurica seedlings to

flooding. Tree Physiol 15:713–719

Zhao Y-J, Hosoya T, Baral H-O, Hosaka K, Kakishima M (2012)

Hymenoscyphus pseudoalbidus, the correct name for Lamber-

tella albida reported from Japan. Mycotaxon 122:25–41

Zheng H-D, Zhuang W-Y (2013) Hymenoscyphus albidoides sp. nov.

and H. pseudoalbidus from China. Mycol Prog. doi:10.1007/

s11557-013-0945-z

Zhu J, Li X, Liu Z, Cao W, Gonda Y, Matsuzaki T (2006) Factors,

affecting the snow and wind induced damage of a montane

secondary forest in Northeastern China. Silva Fennica

40(1):37–51

Zhu J, Mao Z, Hu L, Zhang J (2007) Plant diversity of secondary

Forests in response to anthropogenic disturbance levels in

montane regions of northeastern China. J For Res 12(6):403–416

Eur J Forest Res

123